Antagonistic Pleiotropy, Mortality Source Interactions, and the Evolutionary Theory of Senescence

Abstract

Most theoretical work on the evolution of senescence has assumed that all individuals within a population are equally susceptible to extrinsic sources of mortality. An influential qualitative prediction based on this assumption is Williams's hypothesis, which states that more rapid senescence is expected to evolve when the magnitude of such extrinsic mortality sources is increased. Much evidence suggests, however, that for many groups of organisms externally imposed mortality risk is a function of an organism's internal condition and hence susceptibility to such hazards. Here we use a model of antagonistic pleiotropy to investigate the consequences that such interactions (between environmental hazard and internal condition) can have for Williams's hypothesis. As with some previous theory examining noninteractive extrinsic mortality sources, we find that an increase in interactive extrinsic sources of mortality makes it less likely that an individual will survive from birth to any given age, weakening selection against physiological deterioration at all ages and thus favoring more rapid senescence. However, an increase in interactive mortality sources also typically strengthens selection against physiological deterioration at any age, given an individual has survived to that age, because it reduces the fitness of poor-condition individuals more than good-condition individuals. These opposing effects are not felt equally at all ages, with the latter predominating at early ages. The combined effects can therefore result in the novel prediction that an increase in interactive extrinsic mortality sources can select for slower senescent deterioration early in life but more rapid deterioration late in life.

Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate

“…In support of previously formulated [63,64] and tested [65] hypotheses, our results suggest that lifespan is determined at population-level by an interaction of intrinsic mortality rates with environmental influences. Condition-dependent EM can cause selection to favour improved somatic maintenance [60,63,65,68] that increases predator-avoidance success and lifespan and permits the manifestation of physiological ageing only in the absence of extrinsic hazard.…”

“…Unlike in species with low EM rates, this interaction probably eliminates individuals from the natural population before they show FS. The interplay of FS, selective disappearance of individuals in an inferior condition and EM rate is probably a universal process [63][64][65], but its detection under natural conditions is challenging. While captive research is vital for understanding mechanisms of senescence, information gained from captivity may be of limited relevance for wild animals in species whose life histories are evolutionarily shaped by high EM.…”

“…While captive research is vital for understanding mechanisms of senescence, information gained from captivity may be of limited relevance for wild animals in species whose life histories are evolutionarily shaped by high EM. Despite high EM rates and AS, condition-dependent mortality may even lead to negligible FS under natural conditions [63,66].…”

A Life-History Model of Human Fitness Indicators

“…The fitness-enhancing effects of any such character are therefore age-dependent and will decrease the longer the character is expressed (Williams & Day, 2003). This tends to lead to selection operating more strongly on individuals when they are at or near peak reproductive age (younger) at a cost to overall longevity.…”

The evolution of aging phenotypes in snakes: a review and synthesis with new data

“…A recent revision of evolutionary aging theory counters the prediction that high-mortality environments will always lead to rapid senescence, phenotypic breakdown, and short life (Williams and Day 2003). Specifically, evolution in high-mortality environments may be expected to lead to long lifespans when the survival of individuals is dependent on condition.…”